ApoE isoform- and microbiota-dependent progression of neurodegeneration in a mouse model of tauopathy

Tau-mediated neurodegeneration is a hallmark of Alzheimer's disease. Primary tauopathies are characterized by pathological tau accumulation and neuronal and synaptic loss. Apolipoprotein E (ApoE)-mediated neuroinflammation is involved in the progression of tau-mediated neurodegeneration, and em...

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Published in:	Science (American Association for the Advancement of Science) Vol. 379; no. 6628; p. eadd1236
Main Authors:	Seo, Dong-Oh, O'Donnell, David, Jain, Nimansha, Ulrich, Jason D, Herz, Jasmin, Li, Yuhao, Lemieux, Mackenzie, Cheng, Jiye, Hu, Hao, Serrano, Javier R, Bao, Xin, Franke, Emily, Karlsson, Maria, Meier, Martin, Deng, Su, Desai, Chandani, Dodiya, Hemraj, Lelwala-Guruge, Janaki, Handley, Scott A, Kipnis, Jonathan, Sisodia, Sangram S, Gordon, Jeffrey I, Holtzman, David M
Format:	Journal Article
Language:	English
Published:	United States 13.01.2023
Subjects:	Animals Anti-Bacterial Agents - pharmacology Apolipoproteins E - genetics Apolipoproteins E - metabolism Disease Models, Animal Gastrointestinal Microbiome - drug effects Gastrointestinal Microbiome - physiology Humans Mice Mice, Transgenic Neuroinflammatory Diseases - genetics Neuroinflammatory Diseases - metabolism Neuroinflammatory Diseases - microbiology Sex Factors tau Proteins - genetics tau Proteins - metabolism Tauopathies - genetics Tauopathies - metabolism Tauopathies - microbiology
ISSN:	1095-9203, 1095-9203
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Abstract	Tau-mediated neurodegeneration is a hallmark of Alzheimer's disease. Primary tauopathies are characterized by pathological tau accumulation and neuronal and synaptic loss. Apolipoprotein E (ApoE)-mediated neuroinflammation is involved in the progression of tau-mediated neurodegeneration, and emerging evidence suggests that the gut microbiota regulates neuroinflammation in an APOE genotype-dependent manner. However, evidence of a causal link between the microbiota and tau-mediated neurodegeneration is lacking. In this study, we characterized a genetically engineered mouse model of tauopathy expressing human ApoE isoforms reared under germ-free conditions or after perturbation of their gut microbiota with antibiotics. Both of these manipulations reduced gliosis, tau pathology, and neurodegeneration in a sex- and ApoE isoform-dependent manner. The findings reveal mechanistic and translationally relevant interrelationships between the microbiota, neuroinflammation, and tau-mediated neurodegeneration.
AbstractList	Tau-mediated neurodegeneration is a hallmark of Alzheimer's disease. Primary tauopathies are characterized by pathological tau accumulation and neuronal and synaptic loss. Apolipoprotein E (ApoE)-mediated neuroinflammation is involved in the progression of tau-mediated neurodegeneration, and emerging evidence suggests that the gut microbiota regulates neuroinflammation in an APOE genotype-dependent manner. However, evidence of a causal link between the microbiota and tau-mediated neurodegeneration is lacking. In this study, we characterized a genetically engineered mouse model of tauopathy expressing human ApoE isoforms reared under germ-free conditions or after perturbation of their gut microbiota with antibiotics. Both of these manipulations reduced gliosis, tau pathology, and neurodegeneration in a sex- and ApoE isoform-dependent manner. The findings reveal mechanistic and translationally relevant interrelationships between the microbiota, neuroinflammation, and tau-mediated neurodegeneration.Tau-mediated neurodegeneration is a hallmark of Alzheimer's disease. Primary tauopathies are characterized by pathological tau accumulation and neuronal and synaptic loss. Apolipoprotein E (ApoE)-mediated neuroinflammation is involved in the progression of tau-mediated neurodegeneration, and emerging evidence suggests that the gut microbiota regulates neuroinflammation in an APOE genotype-dependent manner. However, evidence of a causal link between the microbiota and tau-mediated neurodegeneration is lacking. In this study, we characterized a genetically engineered mouse model of tauopathy expressing human ApoE isoforms reared under germ-free conditions or after perturbation of their gut microbiota with antibiotics. Both of these manipulations reduced gliosis, tau pathology, and neurodegeneration in a sex- and ApoE isoform-dependent manner. The findings reveal mechanistic and translationally relevant interrelationships between the microbiota, neuroinflammation, and tau-mediated neurodegeneration. Tau-mediated neurodegeneration is a hallmark of Alzheimer's disease. Primary tauopathies are characterized by pathological tau accumulation and neuronal and synaptic loss. Apolipoprotein E (ApoE)-mediated neuroinflammation is involved in the progression of tau-mediated neurodegeneration, and emerging evidence suggests that the gut microbiota regulates neuroinflammation in an APOE genotype-dependent manner. However, evidence of a causal link between the microbiota and tau-mediated neurodegeneration is lacking. In this study, we characterized a genetically engineered mouse model of tauopathy expressing human ApoE isoforms reared under germ-free conditions or after perturbation of their gut microbiota with antibiotics. Both of these manipulations reduced gliosis, tau pathology, and neurodegeneration in a sex- and ApoE isoform-dependent manner. The findings reveal mechanistic and translationally relevant interrelationships between the microbiota, neuroinflammation, and tau-mediated neurodegeneration.
Author	Meier, Martin Franke, Emily Karlsson, Maria O'Donnell, David Deng, Su Handley, Scott A Lelwala-Guruge, Janaki Desai, Chandani Kipnis, Jonathan Seo, Dong-Oh Gordon, Jeffrey I Ulrich, Jason D Lemieux, Mackenzie Hu, Hao Bao, Xin Cheng, Jiye Jain, Nimansha Sisodia, Sangram S Holtzman, David M Serrano, Javier R Dodiya, Hemraj Herz, Jasmin Li, Yuhao
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School of Medicine, St. Louis, MO, USA – sequence: 5 givenname: Jasmin surname: Herz fullname: Herz, Jasmin organization: Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA – sequence: 6 givenname: Yuhao orcidid: 0000-0003-2413-0937 surname: Li fullname: Li, Yuhao organization: Division of Infectious Diseases, Department of Medicine, Washington University School of Medicine, St. Louis, MO, USA – sequence: 7 givenname: Mackenzie orcidid: 0000-0001-6015-8668 surname: Lemieux fullname: Lemieux, Mackenzie organization: Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA – sequence: 8 givenname: Jiye orcidid: 0000-0002-0266-3997 surname: Cheng fullname: Cheng, Jiye organization: The Edison Family Center for Genome Sciences and Systems Biology and the Center for Gut Microbiome and Nutrition Research, Washington University School of Medicine, St. Louis, MO, USA – sequence: 9 givenname: Hao surname: Hu fullname: Hu, Hao organization: Department of Neurology, Hope Center for Neurological Disorders, Washington University School of Medicine, St. Louis, MO, USA – sequence: 10 givenname: Javier R orcidid: 0000-0002-5937-0212 surname: Serrano fullname: Serrano, Javier R organization: Department of Neurology, Hope Center for Neurological Disorders, Washington University School of Medicine, St. Louis, MO, USA – sequence: 11 givenname: Xin surname: Bao fullname: Bao, Xin organization: Department of Neurology, Hope Center for Neurological Disorders, Washington University School of Medicine, St. Louis, MO, USA – sequence: 12 givenname: Emily orcidid: 0000-0002-0887-957X surname: Franke fullname: Franke, Emily organization: Department of Neurology, Hope Center for Neurological Disorders, Washington University School of Medicine, St. Louis, MO, USA – sequence: 13 givenname: Maria surname: Karlsson fullname: Karlsson, Maria organization: The Edison Family Center for Genome Sciences and Systems Biology and the Center for Gut Microbiome and Nutrition Research, Washington University School of Medicine, St. Louis, MO, USA – sequence: 14 givenname: Martin surname: Meier fullname: Meier, Martin organization: The Edison Family Center for Genome Sciences and Systems Biology and the Center for Gut Microbiome and Nutrition Research, Washington University School of Medicine, St. Louis, MO, USA – sequence: 15 givenname: Su surname: Deng fullname: Deng, Su organization: The Edison Family Center for Genome Sciences and Systems Biology and the Center for Gut Microbiome and Nutrition Research, Washington University School of Medicine, St. Louis, MO, USA – sequence: 16 givenname: Chandani orcidid: 0000-0002-3708-3634 surname: Desai fullname: Desai, Chandani organization: The Edison Family Center for Genome Sciences and Systems Biology and the Center for Gut Microbiome and Nutrition Research, Washington University School of Medicine, St. Louis, MO, USA – sequence: 17 givenname: Hemraj orcidid: 0000-0002-0908-0014 surname: Dodiya fullname: Dodiya, Hemraj organization: Department of Neurobiology, The University of Chicago, Chicago, IL, USA – sequence: 18 givenname: Janaki surname: Lelwala-Guruge fullname: Lelwala-Guruge, Janaki organization: The Edison Family Center for Genome Sciences and Systems Biology and the Center for Gut Microbiome and Nutrition Research, Washington University School of Medicine, St. Louis, MO, USA – sequence: 19 givenname: Scott A orcidid: 0000-0002-2143-6570 surname: Handley fullname: Handley, Scott A organization: Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA – sequence: 20 givenname: Jonathan orcidid: 0000-0002-3714-517X surname: Kipnis fullname: Kipnis, Jonathan organization: Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA – sequence: 21 givenname: Sangram S orcidid: 0000-0002-4039-8864 surname: Sisodia fullname: Sisodia, Sangram S organization: Department of Neurobiology, The University of Chicago, Chicago, IL, USA – sequence: 22 givenname: Jeffrey I orcidid: 0000-0001-8304-3548 surname: Gordon fullname: Gordon, Jeffrey I organization: Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA – sequence: 23 givenname: David M orcidid: 0000-0002-3400-0856 surname: Holtzman fullname: Holtzman, David M organization: Knight Alzheimer Disease Research Center, Washington University School of Medicine, St. Louis, MO, USA
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Snippet	Tau-mediated neurodegeneration is a hallmark of Alzheimer's disease. Primary tauopathies are characterized by pathological tau accumulation and neuronal and...
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SubjectTerms	Animals Anti-Bacterial Agents - pharmacology Apolipoproteins E - genetics Apolipoproteins E - metabolism Disease Models, Animal Gastrointestinal Microbiome - drug effects Gastrointestinal Microbiome - physiology Humans Mice Mice, Transgenic Neuroinflammatory Diseases - genetics Neuroinflammatory Diseases - metabolism Neuroinflammatory Diseases - microbiology Sex Factors tau Proteins - genetics tau Proteins - metabolism Tauopathies - genetics Tauopathies - metabolism Tauopathies - microbiology
Title	ApoE isoform- and microbiota-dependent progression of neurodegeneration in a mouse model of tauopathy
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